The Vitamin E analog Trolox reduces copper toxicity in the annelid Lumbriculus variegatus but is also toxic on its own

NeuroToxicology

Volumn 27, Issue 4, 2006, Pages 604-614

  O'Gara, Bruce A ^a   Murray, Phillip M ^a   Hoyt, Erik M ^a   Leigh Logan, Tifany ^a   Smeaton, Michael B ^a  

^a HUMBOLDT STATE UNIVERSITY   (United States)

Author keywords

Antioxidant; Behavior; Metals; Neurophysiology; Reactive oxygen species

Indexed keywords

ALPHA TOCOPHEROL DERIVATIVE; ANTIOXIDANT; COPPER; TROLOX C;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANNELID WORM; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; GIANT NERVE CELL; LC 50; LOCOMOTION; MUSCLE POTENTIAL; NERVE CONDUCTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; TACTILE STIMULATION;

ANALYSIS OF VARIANCE; ANIMALS; CHROMANS; COPPER; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION ROUTES; DRUG INTERACTIONS; DRUG TOXICITY; ELECTROMYOGRAPHY; LETHAL DOSE 50; MOVEMENT; MUSCLES; NERVE FIBERS; NEURAL CONDUCTION; OLIGOCHAETA; SWIMMING;

ANNELIDA; LUMBRICULUS; LUMBRICULUS VARIEGATUS;

EID: 33744996947     PISSN: 0161813X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuro.2006.03.023     Document Type: Article

References (56)

1. Baatrup E. Structural and functional effects of heavy metals on the nervous system, including sense organs, of fish. Comp Biochem Physiol 100C (1991) 253-257
2. Barceloux D.G. Copper. J Toxicol Clin Toxicol 37 (1999) 217-230
3. Bast A., and Haenen G.R.M.M. The toxicity of antioxidants and their metabolites. Environ Toxicol Pharmacol 11 (2002) 251-258
4. Burkitt M.J. A critical overview of the chemistry of copper-dependent low density lipoprotein oxidation: roles of lipid hydroperoxides, α-tocopherol, thiols, and ceruloplasmin. Arch Biochem Biophys 394 (2001) 117-135
5. Burkitt M.J., and Milne L. Hydroxyl radical formation from Cu(II)-Trolox mixtures: insights into the pro-oxidant properties of α-tocopherol. FEBS Lett 379 (1996) 51-54
6. Calviello G., Di Nicuolo F., Piccioni E., Marcocci M.E., Serini S., Maggiano N., et al. γ-Tocopheryl quinone induces apoptosis in cancer cells via caspase-9 activation and cytochrome c release. Carcinogenesis 24 (2003) 427-433
7. Campbell A., Smith M.A., Sayre L.M., Bondy S.C., and Perry G. Mechanisms by which metals promote events connected to neurodegenerative diseases. Brain Res Bull 55 (2001) 125-132
8. Chapman K.K., Benton M.J., Brinkhurst R.O., and Scheuerman P.R. Use of the aquatic oligochaetes Lumbriculus variegatus and Tubifex tubifex for assessing the toxicity of copper and cadmium in a spiked-artificial-sediment toxicity test. Environ Toxicol 14 (1999) 271-278
9. Cornwell D.G., Williams M.V., Wani A.A., Wani G., Shen E., and Jones K.H. Mutagenicity of tocopheryl quinones: evolutionary advantage of selective accumulation of dietary α-tocopherol. Nutr Cancer 43 (2002) 111-118
10. Dawson T.D., Lott K.G., Leonard E.N., and Mount D.R. Time course of metal loss in Lumbriculus variegatus following sediment exposure. Environ Toxicol Chem 22 (2003) 886-889
11. Diaz Z., Colombo M., Mann K.K., Su H., Smith K.N., Bohle D.S., et al. Trolox selectively enhances arsenic-mediated oxidative stress and apoptosis in APL and other malignant cell lines. Blood 105 (2005) 1237-1245
12. Ding J., Drewes C.D., and Hsu W.H. Behavioral effects of ivermectin in a freshwater oligochaete, Lumbriculus variegatus. Environ Toxicol Chem 20 (2001) 1584-1590
13. Drewes C.D. Escape reflexes in earthworms and other annelids. In: Eaton R.C. (Ed). Neural mechanisms of startle behavior (1984), Plenum Press, New York 43-91
14. Drewes C.D. Helical swimming and body reversal behaviors in Lumbriculus variegatus (Annelida: Clitellata: Lumbriculidae). Hydrobiologia 406 (1999) 263-269
15. Drewes C.D., and Fourtner C.R. Hindsight and rapid escape in a freshwater oligochaete. Biol Bull 177 (1989) 363-371
16. Drewes C.D., McFall J.L., Vining E.P., and Pallas S.L. Longitudinal variations in MGF-mediated giant motor neuron activity and rapid escape shortening in intact earthworms. Comp Biochem Physiol 67A (1980) 659-665
17. Driver C., and Georgeou A. Variable effects of vitamin E on Drosophila longevity. Biogerontology 4 (2003) 91-95
18. Eaton J.W., and Qian M. Interaction of copper with glycated proteins: possible involvement in the etiology of diabetic neuropathy. Mol Cell Biochem 234/235 (2002) 135-142
19. Erdélyi L., Kovács T., Insperger K., and Földesi Zs. Pharmacological actions of essential (zinc, copper) and toxic metal ions (lead, mercury) on neurons and neuronal synapses of the snail, Helix pomatia L. Neurotoxicology 19 (1998) 565-570
20. Gaetke L.M., and Chow C.K. Copper toxicity, oxidative stress, and antioxidant nutrients. Toxicology 189 (2003) 147-163
21. Günther J. Zur Organisation der exteroceptiven Afferenzen in den Korpersegmenten des Regenwurms. Verh Dtsch Zool Ges 64 (1970) 261-265
22. Günther J. Giant motor neurons in the earthworm. Comp Biochem Physiol 42 (1972) 967-974
23. Gyulkhandanyan A.V., Feeney C.J., and Pennefather P.S. Modulation of mitochondrial membrane potential and reactive oxygen species production by copper in astrocytes. J Neurochem 87 (2003) 448-460
24. Hamilton M.A., Russo R.C., and Thurston R.V. Trimmed Spearman-Karber method for estimating median lethal concentration in toxicity bioassays. Environ Sci Technol 11 (1977) 714-719. http://www.epa.gov/ceampubl/fchain/lc50/index.htm [Correction: 1978; 12:417. Computer program available at: http://www.epa.gov/ceampubl/fchain/lc50/index.htm]
25. Hawkins R.L., Mori M., Inoue M., and Torii K. Proline, ascorbic acid, or thioredoxin affect jaundice and mortality in Long Evans cinnamon rats. Pharmacol Biochem Behav 52 (1995) 509-515
26. Horning M.S., and Trombley P.Q. Zinc and copper influence excitability of rat olfactory bulb neurons by multiple mechanisms. J Neurophysiol 86 (2001) 1652-1660
27. Iwasaki K., and Sato M. Inhibitory effects of some heavy metal ions on taste nerve responses in mice. Jpn J Physiol 34 (1984) 907-918
28. Ko K.M., Yick P.K., Poon M.K.T., and Ip S.P. Prooxidant and antioxidant effects of Trolox on ferric ion-induced oxidation of erythrocyte membrane lipids. Mol Cell Biochem 141 (1994) 65-70
29. Komulainen H., and Tuomisto J. Effect of copper on the uptake and release of monoamines in rat brain synaptosomes. Acta Pharmacol Toxicol 48 (1981) 205-213
30. 3 receptor-mediated ion current by divalent metal cations in NCB-20 neuroblastoma cells. J Neurophysiol 66 (1991) 1329-1337
31. A receptor-channel complex by polyvalent cations in rat dorsal root ganglion neurons. Brain Res 607 (1993) 222-232
32. Marchioli R., Schweiger C., Levantesi G., Tavazzi L., and Valagussa F. Antioxidant vitamins and prevention of cardiovascular disease: epidemiological and clinical trial data. Lipids 36 (2001) S53-S63
33. Meyer J.S., Boese C.J., and Collyard S.A. Whole-body accumulation of copper predicts acute toxicity to an aquatic oligochaete (Lumbriculus variegatus) as pH and calcium are varied. Comp Biochem Physiol 133C (2002) 99-109
34. Miller E.R., Pastor-Barriuso R., Dalal D., and Riemersma R.A. Meta-analysis: high-dosage vitamin E supplementation may increase all-cause mortality. Ann Intern Med 142 (2005) 37-46
35. Mizutani K., Shimoi S., Ogawa H., Kitamura Y., and Oka K. Modulation of motor patterns by sensory feedback during earthworm locomotion. Neurosci Res 48 (2004) 457-462
36. Morley A.A., and Trainor K.J. Lack of an effect of vitamin E on lifespan of mice. Biogerontology 2 (2001) 109-112
37. O'Gara B.A., Bohannon V.K., Teague M.W., and Smeaton M.B. Copper-induced changes in locomotor behaviors and neuronal physiology of the freshwater oligochaete, Lumbriculus variegatus. Aquat Toxicol 69 (2004) 51-66
38. O'Gara B.A., Vining E.P., and Drewes C.D. Electrophysiological correlates of rapid escape reflexes in intact earthworms, Eisenia foetida. I. Functional development of giant nerve fibers during embryonic and postembryonic periods. J Neurobiol 13 (1982) 337-353
39. Phipps G.L., Mattson V.R., and Ankley G.T. Relative sensitivity of three freshwater benthic macroinvertebrates to ten contaminants. Arch Environ Contam Toxicol 28 (1995) 281-286
40. 2+. Toxicology 143 (2000) 263-273
41. Rietjens I.M.C.M., Boersma M.G., de Haan L., Spenkelink B., Awad H.M., Cnubben N.H.P., et al. The pro-oxidant chemistry of the natural antioxidants vitamin C, vitamin E, carotenoids and flavonoids. Environ Toxicol Pharmacol 11 (2002) 321-333
42. Rogge R.W., and Drewes C.D. Assessing sublethal neurotoxicity effects in the freshwater oligochaete, Lumbriculus variegatus. Aquat Toxicol 26 (1993) 73-90
43. Rotilio G., Carri M.T., Rossi L., and Ciriolo M.R. Copper-dependent oxidative stress and neurodegeneration. IUBMB Life 50 (2000) 309-314
44. Salánki J., Budai D., Hiripi L., and Kása P. Acetylcholine level in the brain and other organs of the bivalve Anodonta cygnea L. and its modification by heavy metals. Acta Biol Hung 44 (1993) 21-24
45. Sandahl J.F., Baldwin D.H., Jenkins J.J., and Scholz N.L. Odor-evoked field potentials as indicators of sublethal neurotoxicity in juvenile coho salmon (Oncorhynchus kisutch) exposed to copper, chlorpyrifos, or esfenvalerate. Can J Fish Aquat Sci 61 (2004) 404-413
46. Schubauer-Berigan M.K., Dierkes J.R., Monson P.D., and Ankley G.T. pH-Dependent toxicity of Cd, Cu, Ni, Pb and Zn to Ceriodaphnia dubia, Pimephales promelas, Hyalella azteca and Lumbriculus variegatus. Environ Toxicol Chem 12 (1993) 1261-1266
47. Smith P.H., and Mittenthal J.E. Intersegmental variation of afferent pathways to giant interneurons of the earthworm, Lumbricus terrestris L. J Comp Physiol A 140 (1980) 351-353
48. Tapiero H., Townsend D.M., and Tew K.D. Trace elements in human physiology and pathology. Copper. Biomed Pharmacother 57 (2003) 386-398
49. Thorton D.E., Jones K.H., Jiang Z., Zhang H., Liu G., and Cornwell D.G. Antioxidant and cytotoxic tocopheryl quinones in normal and cancer cells. Free Radic Biol Med 18 (1995) 963-976
50. Trombley P.Q., Horning M.S., and Blakemore L.J. Carnosine modulates zinc and copper effects on amino acid receptors and synaptic transmission. Neuroreport 9 (1998) 3503-3507
51. Veltz-Balatre I. Contribution à l'étude, chez un invertébré d'eau douce: Lumbriculus variegatus (Annélide, Oligochète), de la toxicité de divers contaminants de l'environnement champardennais. Bull Soc Zool Fr 125 (2000) 333-341
52. Veltz-Balatre I., Biagianti-Risbourg S., and Vernet G. De la regeneration céphalique de l'oligochaete Lumbriculus variegatus Müller à l'étude de la toxicité des métaux lourds. Année Biol 39 (2000) 39-52
53. 2+-dependent neurotransmitter release from brain catecholaminergic nerve terminals. Eur J Pharmacol 373 (1999) 163-169
54. Yamazaki K., Ohyama H., Kurata K., and Wakabayashi T. Effects of dietary vitamin E on clinical course and plasma glutamic oxaloacetic transaminase and glutamic pyruvic transaminase activities in hereditary hepatic LEC rats. Lab Anim Sci 43 (1993) 61-67
55. Zingg J.-M., and Azzi A. Non-antioxidant activities of vitamin E. Curr Med Chem 11 (2004) 1113-1133
56. Zoran M.J., and Drewes C.D. Rapid escape reflexes in aquatic oligochaetes: variations in design and function of evolutionarily conserved giant fiber systems. J Comp Physiol A 161 (1987) 729-738